Evolution of ontogeny in the hippopotamus skull: using allometry to dissect developmental change

Allometry describes the effect of size change on aspects of an organism's form and can be used to summarize the developmental history of growing parts of an animal. By comparing how allometric growth differs between species, it is possible to reveal differences in their pathways of development. The ability to compare and categorize developmental change between species is demonstrated here using morphometric methods. This involves the interspecific statistical comparison of a large number of bivariate relationships that summarize ontogenetic trajectories. These linear ontogenetic trajectories can be modified as they evolve in any of three ways: ontogenetic scaling indicative of change in the duration of growth, lateral shifts indicative of changes in prenatal development, and directional change indicative of novel modes of postnatal growth. I apply this analysis to skulls of the common hippopotamus ( Hippopotamus amphibius ) and the pygmy hippopotamus ( Hexaprotodon liberiensis ). The number of allometric changes falling into each category was statistically determined and Jolicoeur's multivariate generalization of simple allometry was used to provide an overview of cranial variation. For these skulls, directional change was not found to be statistically significant, but ontogenetic scaling and lateral shifts were both common. This indicates that conserved patterns of growth covariance (ontogenetic scaling) can be separated from novel or derived patterns (directional change and/or lateral shifts). This study demonstrates that He. liberiensis is not simply an ontogenetically scaled version of its larger relative. The evolutionary implications of allometric growth variation are discussed in the light of these findings and those of other studies.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 625–638.     

Variation in the digging apparatus of the subterranean silvery mole-rat, Heliophobius argenteocinereus (Rodentia, Bathyergidae): the role of ecology and geography

The skull of most subterranean tooth-digging rodents is markedly affected by their digging mode. In the present study, we investigated the cranial variation in a strictly subterranean, highly specialized Afrotropical tooth-digger, Heliophobius argenteocinereus (Bathyergidae, Rodentia), using a geometric morphometric approach and evaluated the effect of different factors on size and shape differences among four populations. No evidence for sexual dimorphism was found in skull size or shape. The cranial shape variation was large and influenced mainly by the type of habitat (miombo woodland versus farmland and grassland) and the latitudinal gradient. The dorsal side of the skull appears to be more plastic and adaptable to local environments, as well as more independent of size, than the ventral side. Only the shortening of the rostrum is presumably an adaptive process independent of size that leads to an increase of efficacy of the tooth-digging apparatus in Heliophobius , whereas the increase in the in-force and the more procumbent incisors both comprise size-related changes caused by ontogenetic allometric growth.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 822–831.     

A test for negative frequency-dependent mating success as a function of male colour pattern in the bluefin killifish

Rare male mating advantage (a form of negative frequency dependence) is frequently proposed as a mechanism for the maintenance of genetic variation within populations. This hypothesis is attractive for systems with pronounced male colour polymorphism because it can maintain particularly high levels of variation. We tested for negative frequency-dependent mating success between yellow and red male colour patterns in bluefin killifish, Lucania goodei . Lucania goodei populations harbour substantial colour pattern polymorphism, and a large proportion of this variation has a genetic basis. We established outdoor mesocosms with red and yellow males in three different ratios: yellow rare (one yellow ♂ : five red ♂), even (three yellow ♂ : three red ♂), and red rare (five yellow ♂ : one red ♂). We obtained eggs and used microsatellites to determine paternity. By contrast to expectations, we found no support for a rare male mating advantage. Red males had slightly higher spawning success than yellow males, particularly in replicates with large clutches and when red males were rare. However, yellow males did not have higher mating success when rare. We discuss alternative mechanisms for the maintenance of the polymorphism as well as the potential reasons for the lack of a rare male mating advantage.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 489–500.     

Species' diversity in the New Caledonian endemic genera Cephalidiosus and Nobarnus (Insecta: Heteroptera: Tingidae), an approach using phylogeny and species' distribution modelling

The patterns of local endemism in New Caledonia were analysed in two endemic genera of Tingidae (Insecta, Heteroptera), Cephalidiosus and Nobarnus , through a phylogenetic analysis and species' distribution modelling. The aim was to determine the possible causes of diversification and endemism in New Caledonia. Our results show that environmental conditions are probably important for the distribution of the genus Cephalidiosus , in conjunction with other factors such as resource (host plant) distribution, but suggest that the same environmental conditions have not influenced the speciation processes and diversification in the genus.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 177–184.     

Local adaptation in a plant herbivore interaction depends on the spatial scale

Local adaptation has central importance in the understanding of co-evolution, maintenance of sexual reproduction, and speciation. We investigated local adaptation in the alkaloid-bearing legume Crotalaria pallida and its seed predator, the arctiid moth Utetheisa ornatrix , at different spatial scales. When we studied three populations from south-east Brazil (150 km apart), we did not find evidence of local adaptation, although we did find interpopulational differences in herbivore performance, and a significant interaction between herbivore sex and plant population. These results indicate that both moth and plant populations are differentiated at the regional scale. In a comparison of populations from Brazil and Florida, the herbivore showed local adaptation to its host plant; for both moth populations, the pupae were heavier when the larvae ate the sympatric than the allopatric host population. We discuss the scale dependence of our results and the possible causes for the lack of local adaptation at the regional scale, even in the presence of plant and moth differentiation. The results obtained demonstrate the importance of studying co-evolution and local adaptation at different geographical scales.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 494–502.     

Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics

Podarcis bocagei and Podarcis carbonelli are two lacertid species endemic to the western Iberian Peninsula, and both show head size and shape sexual dimorphism. We studied immature and adult head sexual dimorphism and analysed ontogenetic trajectories of head traits with body and head size, aiming to shed light on the proximate mechanisms involved. Immatures were much less dimorphic than adults, but geometric morphometric techniques revealed that head shape sexual differences are already present at this stage. Males and females differed in allometry of all head characters with body size, with males showing a disproportionate increase of head size and dimensions. On the other hand, head dimensions and head shape changed with increasing head size following similar trends in both sexes, possibly indicating developmental restrictions. Consequently, adult sexual dimorphism for head characters in these species is the result of both shape differences in the immature stage and hypermetric growth of the head in relation to body size in males.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 111–124.     

Species: towards new, well-grounded practices

Velasco recently criticized our formal definition of the species concept, arguing for its inappropriateness both in fundamental and practical aspects [Velasco JD (2008) Biological Journal of the Linnean Society , 93 , 865–869]. Here, we clarify some misunderstandings that are at the basis of Velasco's paper. First, we show why and how the definition of the species concept can be grounded in the theory of evolution and what that implies. Then, we explain why Velasco's formal criticisms are unjustified. Finally, we point out the practical and methodological consequences of a rigorous conceptual framework for species study, and we show that today's development of species delimitation methods fully agrees with our proposal.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 217–222.     

Inter-annual variation and information content of melanin-based coloration in female Eurasian kestrels

Competition for resources (e.g. mates or food) is the main evolutionary explanation for conspicuous ornaments in males, although this idea is not generalized in females. Whether or not the expression of melanic coloration is dependent on environmental conditions remains controversial. We studied three different melanin-based female traits in the Eurasian kestrel Falco tinnunculus , a sexually dichromatic species, for a period of 10 years: grey coloration in rump and tail and the width of the black subterminal tail band. We analysed these traits for within-individual variation among years, as well as their possible link with indices of quality, such as age, body size, and breeding performance. The results obtained demonstrate that female melanin-based coloration increased from yearlings to adults. In addition, the expression of female rump coloration covaried positively with the environmental conditions in the previous year (i.e. measured as clutch size at population level). Finally, we found a positive correlation between grey rump coloration and clutch size. These results suggest that the expression of rump coloration, a melanin-based trait, is environmentally constrained, and we propose that this character could function as an indicator of individual quality in female Eurasian kestrels.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 781–790.     

Regressive evolution: ontogeny and genetics of cavefish eye rudimentation

Two hypotheses exist to explain ontogenetic eye reduction in Astyanax cave fish: first, after lens induction by the primordial eye cup, the lens plays the role of a central regulator of eye and retina regression or, second, the retina itself is an independent unit of eye development. A comparative study of five blind cave fish populations and their surface sister form was performed to investigate the differences of ontogenetic eye regression between the cave populations during different stages of development. The study revealed that, in addition to the initial formation of smaller primordia, eye regression is also caused during later ontogeny by different relative growth and specific histological characteristics. Whereas the cave fish lens never properly differentiates, the regressive process of the retina is transitorily interrupted by ongoing differentiation. In the newly-discovered Molino cave population, even visual cells with well-organized outer segments develop, which are secondarily reduced at a later ontogenetic stage. This result shows that the retina and lens are independent developmental units within the eye ball. Presumably, the genetic systems responsible for both show independent inheritance, which is also corroborated by hybrids of F ₂-crosses between the cave and surface fish, in which lens and retina development do not correlate. During ontogeny, the eye size differs between the cave populations. In Pachón cave fish, the relatively large eye size correlates with an ancient introgression from a surface population, which may have delayed eye regression.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 287–296.     

Genetic variation in Irish pygmy shrews Sorex minutus (Soricomorpha: Soricidae): implications for colonization history

The status of the pygmy shrew ( Sorex minutus L.) as a native or an introduced species in Ireland has been subject to much debate. To examine this and other aspects of the colonization history of the Irish pygmy shrew, genetic variation was determined in 247 pygmy shrews collected throughout Ireland, using mitochondrial control region sequences and five polymorphic microsatellite loci. Genetic diversity was low for both types of marker. The median-joining network for control region sequences was star-like, suggesting that the colonization of Ireland involved a small number of founders and rapid population expansion thereafter; this was supported by other statistics. Molecular dating with both mitochondrial DNA and microsatellite data is consistent with a human introduction. This would have been several thousand years ago; a recent colonization within historical times can be ruled out. This is the first detailed population genetic study of the pygmy shrew anywhere in its range.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 918–927.     

Long-term stability of hornet cuticular hydrocarbons facilitates chemotaxonomy using museum specimens

Cuticular hydrocarbons are key compounds used for insect chemical communication and their species-specificity makes them of great utility to chemotaxonomists. However, very little is known about their long-term stability in relation to their use as reliable taxonomic tools. We compared the cuticular hydrocarbon profiles of fresh extracts from four hornet ( Vespa ) species with extracts from specimens that were frozen for 1 year and of those stored in insect display boxes for 20 years. Cuticular hydrocarbon profiles were qualitatively very stable, maintaining their species-specific profiles even after 20 years. The long-term stability of cuticular hydrocarbons in hymenopterans opens up the possibility of using museum collections for chemotaxonomy studies and helping with the delineation of species in difficult groups.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 732–737.     

Seed dormancy and germination behaviour in two Euphrasia species (Orobanchaceae) occurring in the Swiss Alps

The optimal time for germination of a seed depends on environmental conditions of its habitat, the life cycle of the germinating plant, and the conditions for successful establishment, growing and reproduction. We studied the germination behaviour of the alpine annual Euphrasia minima and an alpine ecotype of E. salisburgensis in a lowland garden experiment. Seeds of both species and their hybrids germinated at constant (5 °C) and at varying temperatures (3–10 °C), and never before spring after seed ripening. Germination was spread over 3 years, which suggests that the seeds formed a persistent seed bank. The two species together with E. minima and E. minima hybrids differed significantly in the germination rate in the first and second spring.  © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 156 , 649–656.     

Effects of habitat heterogeneity and local adaptation on the body condition of a forest passerine at the edge of its distributional range

We studied fluctuating asymmetry and feather growth rates as indicators of fitness of blackcaps ( Sylvia atricapilla ) breeding at the border of their distribution range in the Iberian Peninsula. Iberian blackcaps increase their abundance with increasing rainfall and ground cover of brambles. In border habitats, they are sedentary and morphologically different from migrants, suggesting that they could be adapted to peripheral conditions. We tested whether juvenile body condition depends on (1) distance from the centre of the range, (2) mean precipitation or (3) bramble cover. Controlling for environmental variation, we tested for differences between migratory and sedentary populations. Body condition varied across the Iberian gradient in parallel with changes in precipitation. Controlling for this effect, sedentary populations were in better body condition than migratory populations. Our results support the idea that environmental heterogeneity causes fitness to fluctuate across species' ranges, and also that local adaptation may mean that peripheral populations are more than a 'tail end' of the species.  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 479–488.     

Morphology and function of the head in foetal and juvenile Scolecomorphus kirkii (Amphibia: Gymnophiona: Scolecomorphidae)

The external and musculoskeletal morphology of the head is described for an ontogenetic series of the scolecomorphid caecilian Scolecomorphus kirkii . The rostral region of foetuses and juveniles is expanded into large, posterolaterally pointing paraoral processes that are formed by the maxilla. Extraoral teeth are present on the underside of the rostrum and laterally on the paraoral processes. In the foetuses, teeth are covered by epidermal tissue. The endoskeletal part of the foetal skull is largely cartilaginous, but all of the dermal bones, with the exception of the squamosal, are present. The foetal chondrocranium is extensively developed and shows a peculiar, posterolateral process of the nasal capsule that is connected to the trabecula cranii by a transverse bar posterior to the choana, and extends further posterior beyond the level of the posterior end of the pila antotica. Only two mm. adductor mandibulae are present, together with two pterygoideus muscles that insert onto the lower jaw. The palatoquadrate and quadrate of foetuses and juveniles, respectively, are highly mobile. It is suggested that the derived head morphology of Scolecomorphus foetuses and juveniles is an adaptation to specialized postparitive feeding.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 491–504.     

Local adaptation in four Iris species tested in a common-garden experiment

Local adaptation is a commonly observed result of natural selection acting in heterogeneous environment. Common-garden experiments are a method of detecting local adaptation, as well as studying phenotypic plasticity and gradients of traits. The present study aimed to analyse reaction norms of four closely-related Iris species of section Oncocyclus and to identify a role of environmentally-specific natural selection in their plastic responses. The plant vegetative and phenological, as well as performance traits were measured in a full factorial common-garden experiment with three levels of water amount and three soil types. We found a significant effect of species identity on all traits measured. Water amount and soil type affected many of the traits, but soil type did not affect the performance. There was no significant difference in the effect of water amount and soil type on performance as reflected by rhizome growth; in other words, there was no significant genotype × environment interaction for performance. Plasticity levels and directions of response were also similar among the species. We conclude that phenotypic differences among species are of genetic origin, although no adaptive value was demonstrated for them at the time and life-stages 'frame' of this experiment.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 98 , 267–277.     

Relationships between drosophilids (Diptera, Drosophilidae) and the environment in two contrasting tropical vegetations

Although natural populations of drosophilid flies have been the subject of ecological studies, the population ecology of these insects in the tropics is still poorly known. This paper discusses aspects of the relationship between drosophilids and their environment, based on 28 monthly collections made in two contrasting vegetations of the Brazilian Cerrado biome: gallery forest and savanna. Exotic species were found in both types of environment; but 14 of the 30 captured Neotropical species occurred exclusively in the gallery forests, probably because of their climatic stability and greater environmental heterogeneity. Even though some endemic species were more abundant in the dry and cold months, most populations exhibited peaks of abundance in the wet season. The species diversity indexes (H' and D), higher in the dry season, were probably affected by increased evenness at this time of year, when the populations of practically all the species are greatly reduced. As species richness in the savanna vegetation clearly decreased in the dry season, increasing again in the wet season, it is suggested that some drosophilids migrate to the forests when climatic conditions are too stressful in the savannas.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 233–247.     

Physiological variation along a geographical gradient: is growth rate correlated with routine metabolic rate in Rana temporaria tadpoles?

Shorter season length and lower temperature towards higher latitudes and altitudes often select for intraspecific clines in development and growth rates. However, the physiological mechanisms enabling these clines are not well understood. We studied the relationship between routine metabolic rate (RMR) and larval life-history traits along a 1500-km latitudinal gradient across Sweden. In a laboratory common garden experiment, we exposed eight common frog Rana temporaria populations to two experimental temperatures (15 and 18 °C) and measured RMR using flow-through respirometry. We found significant differences among populations in RMR, but there was no evidence for a linear relationship between latitude and RMR in either temperature treatment. However, we found a concave relationship between latitude and RMR at the lower experimental temperature. RMR was not correlated with growth rate at population or at individual levels. The results obtained suggest that, unlike in growth and development rates, there is no latitudinal cline in RMR in R. temporaria tadpoles.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 217–224.     

Differences in environmental predictability underlie divergent competitive abilities in three congeneric hydroids

Species in which individuals experience predictable and uniform environments should be most finely adapted to their environment. Many hydrozoan species in the genus Hydractinia simultaneously occupy similar microhabitats (gastropod shells inhabited by hermit crabs) but experience considerable differences in their immediate environment (size and species of shells and hosts). In the present study, hydroid species experience differences in environmental predictability and traits that mediate competitive ability (growth form and growth rate). The inferred competitive ability was directly proportional to the extent to which the gastropod environment promotes interactions between small, juvenile colonies, which always end in competitive elimination. Extensive intraspecific variation in competitive ability was explained primarily by crab host species or site. Dense host populations impose more severe disturbance regimes that favour competitively inferior, but disturbance-resistant, phenotypes. Interplay between different types of variation (gastropods and hermit crabs) provides a possible mechanism for the maintenance of intraspecific growth form variation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 322–338.     

Coevolution of daily activity timing in a host–parasite system

Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 399–405.